The impacts of phylogenetic methods on taxonomy and conservation

The rise of molecular methods has expanded the scope of biological issues that can be addressed, but has also led to calls for the phylogenetic species concept to be universally adopted. Molecular methods are particularly useful in taxonomy, but also in population genetics and landscape ecology (Haig et al. 2011). Various genetic methods have proved useful in taxonomy; for delineating geographic and evolutionary boundaries of species and subspecies; analysing the

extent of hybridization; deciphering cryptic species; and establishing relationships between species and subspecies (Haig et al. 2011). The increasing use of molecular methods, however, has led to calls for a shift from the biological species concept to some version of the phylogenetic species concept, for example, in avian species (Cracraft 1997) and plant species (Soltis and Gitzendanner 1999).

Changing species concepts can, however, have wide ranging effects on conservation. These include, among other things: 1) the specific status of diagnosable populations, 2) estimates of species diversity, 3) delineation of areas of endemism, 4) decisions on captive breeding, predator control etc., and 5) which units will be given protection under legislation (Cracraft 2000). For instance, a study of the geographic distribution of avian endemism in Mexico found that using either the biological species concept or the phylogenetic species concept produced drastically different maps of species richness endemic to single biotic regions, and consequently altered conservation area priorities (Peterson and Navarro Sigüenza 1999). In follow-up work, Rojas- Soto et al. (2010) compared the 371 species and subspecies on the official list (NOM) of threatened and endangered taxa protected by Mexican legislation compiled using the BSC, with an alternative species level taxonomy using the PSC. They found 298 were concordant forms (protected under both concept), 47 were discordant forms (BSC species or subspecies that did not correspond to PSC recognised species), 28 were under-protected forms (PSC recognised species that are part of a widespread BSC species at a lower threat level), and 11 were

unprotected forms (restricted distribution PSC species). The protection scenarios based on the two concepts showed that the total number of protected forms by risk category (endangered, threatened, special protection) remained statistically the same, however, ‘the major difference between the lists is based on which forms are exclusively protected on each list’ (Rojas-Soto, Navarro-Sigüenza, and de Los Monteros 2010: 181 original emphasis). The major differences arise from the use of subspecies under the BSC, where certain species are shown to have

continuous distribution and clinal variation rather than distinct subspecies. In well studied groups total numbers don’t change dramatically, for example, in New Zealand suggested numbers under a PSC rise from 235-245 (Holdaway, Worthy, and Tennyson 2001), however, in less studied groups the impact of the PSC on numbers of species can be striking.

The use of the phylogenetic species concept has led to increased numbers of species for a range of reasons. In a meta-analysis of 89 studies where organisms (plants, fungus, lichen, birds, mammals, arthropods, retiles, fish etc.) had been classified by both the biological species concept and the phylogenetic species concept Agapow et al. (2004) found that 48.7 per cent more species were recognised under the phylogenetic species concept, with an associated decrease in

suggest that the 48.7 per cent increase in species number ‘infers an average decrease in mature individuals per species of 32.8 per cent’ (Agapow et al. 2004). This rapid increase in the number of endangered species is likely to further strain conservation resources.

The phylogenetic species concept is also particularly likely to be applied to charismatic megafauna, with Isaac et al. (2004) suggesting that the PSC is one of the contributors to

‘taxonomic inflation’ within these taxonomic groups. For instance, the growth in primate species is significantly greater than the level of taxonomic inflation in other well studied groups, and Mace (2004: 714) argues ‘the number of primate species added to the list by taxonomic revision is currently overwhelming changes in the list caused by real changes in conservation status’. Others, however, regard taxonomic inflation as a loaded term for what they see as the necessary

incorporation of evolutionary research into taxonomy, and suggest the situation with primates should be seen as an exception (Knapp, Lughadha, and Paton 2005; Agapow and Sluys 2005). Perhaps a larger problem than taxonomic inflation among some charismatic groups are distinct biases in the attention that some taxonomic groups receive, or what Lorimer (2006) describes as ‘taxonomic partialities’. For instance, Gippoliti and Amori (2007: 113) suggest that even within the class Mammalia ‘discrepancies in the inclusion of subspecies in the IUCN Red List often reflect uneven taxonomic knowledge and the differential scientific and public interest raised by different kinds of mammals, which together can produce a biased picture of mammalian endangerment worldwide’. So, taxonomic research can potentially be driven by the charisma of the group being studied, but this is highly variable within different groups.

There is an intense debate among conservationists between proponents of the biological and phylogenetic species concepts. This debate is complicated by the fact that the conservation body responsible for listing threatened birds (Birdlife International) adopts the BSC and is on the whole conservative about accepting new species until the evidence is very strong, while the IUCN, responsible for mammals, amphibian and fishes allow for species that are spread over discrete habitat patches, and consequently increases the likelihood of taxonomic splitting under the PSC (Mace 2004). Ornithologists, however, have been prominent in promoting a change to the phylogenetic species concept (Cracraft 1997), arguing that ‘taxonomic neglect’ promotes extinction of distinctive endemics because subspecies are so often ignored by biologists and conservationists who rely on the biological species concept (Hazevoet 1996). They also argue that the PSC enables conservationists to precisely identify the basic units of conservation, which should result in a more efficient use of resources (Sangster 2000). Conversely advocates for retaining the BSC for avian species argue that the recognition of too many additional species would draw too much time and money from currently recognised species and would destabilise

taxonomy (Collar 1996; Sutherland 2000). Garnett and Christidis (2007: 189) suggest a sudden surge in species has implications for broader society beyond just conservation;

[E]ach time the name of a species changes, or species boundaries are redefined, a huge bureaucratic process is triggered to update schedules, regulations, maps and publications. This has both transaction and opportunity costs, the former because substantial conservation monies are spent negotiating the new lists through the administrative processes, and the latter because those funds might have been available for genuine on-ground conservation.

Again, it is likely to be the charismatic groups of species that attract phylogenetic analysis, and the question is whether they deserve greater attention than those that have yet to attract the attention of a splitting taxonomist (Sutherland 2000). The resulting arguments have been most heated over the question of subspecies.

The category of subspecies has caused considerable dissatisfaction among taxonomists and biologists. In part, this is because, prior to the advent of statistical and genetic methods,

subspecies names might refer to quite different types of entity; arbitrary points on clines, average differences between populations, zones of intergradation, or diagnosably distinct endemic island taxa, which are not of equivalent importance for conservation (Remsen Jr 2005; Hazevoet 1996). One area that has received attention is whether subspecies named under a biological species concept reflect distinct phylogenetic entities (Zink 2004b; Phillimore and Owens 2006). Zink (2004b) found that only three per cent of North American and European avian subspecies reflected distinct taxonomic entities, and argued traditional non-molecular methods have the potential to misinform conservation efforts through misrepresenting the underlying patterns of intraspecific variation. However, Phillimore and Owens (2006) found that this reflected a continental bias of North American and European subspecies, and when island dwelling

subspecies from around the world were included they found that 36 per cent of avian subspecies were phylogenetically distinct. A widely cited example of the problematic nature of subspecies (usually by those who mistrust traditional taxonomy) concerns the dusky seaside sparrow. This was discovered in 1872 and described as a distinct species Ammodramus nigrescens, which was confined to a small part of eastern Florida (Avise 1989). In 1973 it was demoted to become one of eight subspecies of the seaside sparrow Ammodramus maritimus, which occurred in coastal marshes from Massachusetts to South Texas, and by 1980 the few individuals left were brought into captivity and mated with individuals from the nearby Gulf coast subspecies A. m. peninsulae (Avise and Nelson 1989). Despite the captive breeding effort the last dusky seaside sparrow died in 1987. A subsequent genetic study, however, found that there was a fundamental genetic split between all Atlantic coast populations and all Gulf coast populations, but within this broad split, the putative subspecies were indistinguishable from one another. The captive breeding effort had been fooled into thinking geographical proximity equated with phylogenetic proximity, because it had been misguided by the traditional taxonomy. This situation, in some ways, resembles the

taxonomic story of the white-flippered penguin, which is the subject of Chapter 8, but the penguin’s story also highlights how the imperatives of conservation and ecotourism have influenced the bird’s taxonomy.